Abstract
Previous research has shown high-quality annual bedding plant seedlings can be produced in controlled environments using light-emitting diode (LED) sole-source lighting (SSL). However, when only red and blue radiation are used, a delay in time to flower may be present when seedlings of some long-day species are subsequently finished in a greenhouse. Thus, our objective was to evaluate the effects of various radiation qualities and intensities under SSL on the morphology, nutrient uptake, and subsequent flowering of annual bedding plant seedlings with a long-day photoperiodic response. Coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’) seedlings were grown at radiation intensities of 105, 210, or 315 µmol·m−2·s−1, achieved from LED arrays with radiation ratios (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8). Four-week-old seedlings were subsequently transplanted and grown in a common greenhouse environment. Stem caliper, root dry mass, and shoot dry mass of seedlings generally increased for all three species as the radiation intensity increased from 105 to 315 µmol·m−2·s−1, regardless of radiation quality. Similarly, stem length of all three species was generally shorter as the radiation intensity increased. Macro- and micronutrient concentrations were also generally lower as the radiation intensity increased for all three species. Pansy seedlings grown under R84:FR7:B9 flowered an average of 7 and 5 days earlier than those under R87:B13 and R74:G18:B8, respectively. These results provide information regarding the specific radiation parameters from commercially available LEDs necessary to produce high-quality seedlings under SSL, with radiation intensity appearing to be the dominant factor in determining seedling quality. Furthermore, the addition of far-red radiation can reduce time to flower after transplant and allow for a faster greenhouse turnover of some species with a long-day photoperiodic response.
The production of young plants from seed (plugs) for the annual bedding plant market commonly occurs during winter and early spring (Styer, 2003). However, in northern latitudes, the natural photosynthetic daily light integral (DLI) is not sufficient to produce high-quality young plants in the greenhouse (Lopez and Runkle, 2008; Pramuk and Runkle, 2005). Previous research has shown that a minimum DLI of 10 to 12 mol·m−2·d−1 is recommended to produce high-quality ornamental young plants (Pramuk and Runkle, 2005; Randall and Lopez, 2014). Thus, to efficiently produce seedlings in northern latitudes, where the DLI in the greenhouse can be as low as 1 to 5 mol·m−2·d−1 during winter and early spring, supplemental lighting is recommended (Pramuk and Runkle, 2005). Currently, high-pressure sodium (HPS) lamps are the industry standard for providing supplemental lighting, with a photosynthetic photon flux density (PPFD) of 70 to 90 µmol·m−2·s–1 commonly targeted (Lopez et al., 2017). One alternative to traditional greenhouse production is multilayer or vertical production indoors in repurposed shipping containers, warehouses, or chambers under sole-source lighting (SSL) provided by light-emitting diodes (LEDs). While SSL applications may not be suitable for all crops, young plant production is one area that may benefit substantially from this technology as growers strive to produce a uniform, high-quality crop during months of the year where greenhouse environmental conditions are both unpredictable and unfavorable. Additionally, young plant production may provide one of the most cost-effective applications for SSL due to the small size and high value of plugs and relatively short production cycle (Park and Runkle, 2017).
Previous research has shown that LED SSL in controlled environments is a promising lighting method for the production of annual bedding plant seedlings (Randall and Lopez, 2015; Wollaeger and Runkle, 2014). Specifically, Randall and Lopez (2015) evaluated seedlings of vinca (Catharanthus roseus ‘Titan Red Dark’), impatiens (Impatiens walleriana ‘Super Elfin XP Blue Pearl’), geranium (Pelargonium ×hortorum ‘Bullseye Red’), petunia (Petunia ×hybrida ‘Dreams Midnight’), and French marigold (Tagetes patula ‘Durango Yellow’) under SSL using LEDs providing a red:blue radiation ratio (%) of either 87:13 or 70:30. Generally, they found that seedlings produced under controlled-environment SSL were more compact, darker in foliage color (higher relative chlorophyll content), and had a higher root mass than those produced under greenhouse supplemental lighting or ambient lighting conditions.
Increases in radiation intensity and DLI have been reported to increase seedling quality and decrease subsequent time to flower (TTF) for many bedding plant species (Oh et al., 2010; Pramuk and Runkle, 2005). Seedlings produced under lower DLIs generally show decreased growth rates and possess more water in the plant tissues, ultimately leading to seedlings that growers would refer to as being less “toned” (Faust et al., 2005). For example, Pramuk and Runkle (2005) found that as the DLI increased from 4.1 to 14.2 mol·m−2·d−1 during seedling production, the average shoot dry mass (SDM) per internode increased linearly for celosia (Celosia argentea var. plumosa ‘Gloria Mix’), impatiens ‘Accent Red’, French marigold ‘Bonanza Yellow’, and pansy (Viola ×wittrockiana ‘Crystal Bowl Yellow’).
One of the benefits LEDs provide is the ability to select specific wavelengths of radiation to elicit desired morphological or physiological plant responses. Red wavelengths are most commonly associated with their role in photosynthesis and dry mass accumulation based on their action at the absorption peaks of chlorophylls (Massa et al., 2008). Compared with red radiation, blue wavelengths are believed to be less photosynthetically efficient due to their absorption by pigments other than chlorophyll and resulting low quantum efficiency (Barnes et al., 1993; Cope et al., 2014; Franklin, 2008; Massa et al., 2008). Another reason for the loss in photosynthetic activity may be due to smaller leaf area, which has been observed under high percentages of blue radiation and ultimately leads to decreased radiation interception (Cope et al., 2014). However, this inhibition response to blue wavelengths may be desirable for many crops as a means of controlling excessive growth (Cope et al., 2014; Cosgrove, 1981; Kigel and Cosgrove, 1991; Runkle and Heins, 2001). Thus, LEDs can be manufactured with a variety of plant responses in mind, such as the control of stem elongation or matching the absorbance peaks of photoreceptors involved in photosynthesis (Mitchell et al., 2012).
Additionally, Stutte (2009) found that the phytochrome photostationary state, the relative proportion of the active form to total phytochrome, could be manipulated using LEDs to either initiate earlier flowering or promote continued growth in the vegetative state for photoperiod-sensitive species. Far-red radiation has a significant effect in the processes of stem elongation and flowering (Downs and Thomas, 1982). For example, a deficiency in far-red radiation has often been found to delay flower initiation or development in species with a long-day photoperiodic response such as campanula (Campanula carpatica ‘Blue Clips’), coreopsis (Coreopsis ×grandiflora ‘Early Sunrise’), and pansy ‘Crystal Bowl Yellow’ (Runkle and Heins, 2001). Thus, reductions in radiation intensity as well as the lack of critical wavelengths in environments using SSL may lead to delays in flowering and a reduction in seedling quality for some species.
While limited research has been conducted on the effects of radiation quality for young-plant production in controlled environments under SSL, to our knowledge, no research to date has evaluated how the manipulation of radiation quality across various radiation intensities might further impact bedding plant seedling quality and TTF under SSL conditions. Additionally, by furthering our understanding regarding the impacts of LED SSL on nutrient uptake, a more thorough outlook on how to optimize production within these environments may be provided. We also postulated that the inclusion of far-red radiation during seedling propagation would initiate earlier flowering at finishing for species with a long-day photoperiodic response. Thus, the objective of the study was to evaluate the effects of various radiation qualities and intensities in a SSL environment on the morphology, nutrient uptake, and subsequent flowering of annual bedding plant seedlings.
Materials and Methods
Plant material and germination environment.
Based on their significance to the greenhouse industry and long-day photoperiodic flowering response (Currey et al., 2011; Runkle and Heins, 2001), seeds of coreopsis ‘Sunfire’, pansy ‘Matrix Yellow’, and petunia ‘Purple Wave’ were sown between 8 Oct. 2014 and 8 Jan. 2015 in 288-cell trays (6-mL individual cell volume) using a commercial soilless medium comprised of (by vol.) 65% peat, 20% perlite, and 15% vermiculite (Fafard Super Fine Germinating Mix; Sun Gro Horticulture, Agawam, MA) and germinated under a 16 h photoperiod (0600 to 2200 hr) in a glass-glazed greenhouse at Purdue University, West Lafayette, IN (lat. 40 °N). An environmental control system (Maximizer Precision 10; Priva Computers Inc., Vineland Station, Ontario, Canada) was used to adjust and measure the greenhouse air temperature. Supplemental lighting was provided by 1000-W HPS lamps, and solar PPFD (400–700 nm) was measured by quantum sensors (SQ-110; Apogee Instruments, Inc., Logan, UT) every 15 s and the average was logged every 15 min by a data logger (Model CR1000; Campbell Scientific, Inc., Logan, UT). The mean ± sd DLI and average daily air temperature (ADT) from sowing to hypocotyl emergence were 7.5 ± 1.7 mol·m−2·d−1 and 22.7 ± 0.3 °C, respectively. Trays were regularly misted using clear water to maintain high humidity and soil moisture until germination occurred.
Growth chamber environment.
Upon uniform hypocotyl emergence within each species, plug trays were placed under SSL treatments with a 16 h photoperiod (0600 to 2200 hr) in a walk-in growth chamber (C5 Control System; Environmental Growth Chambers, Chagrin Falls, OH). The air temperature, relative humidity, and CO2 set points were 21 °C, 70/80% day/night (D/N; 16 h/8 h), and 500 µmol·mol−1, respectively. A data logger (DL1 Datalogger; Environmental Growth Chambers) was used to record average air temperature, D/N relative humidity, and CO2 concentration every 15 min, with a mean ± sd of 21.0 ± 0.1 °C, 69.8 ± 0.5% D/79.5 ± 0.5% N, and 499.6 ± 33.1 µmol·mol−1, respectively, across three experimental replications. Seedlings were irrigated daily with water-soluble fertilizer (Jack’s LX 16N–0.94P–12.3K Plug Formula for High Alkalinity Water; J.R. Peters, Inc., Allentown, PA) providing (in mg·L−1): 100 nitrogen (N), 10 phosphorus (P), 78 potassium (K), 18 calcium (Ca), 9.4 magnesium (Mg), 0.10 boron (B), 0.05 copper (Cu), 0.50 iron (Fe), 0.25 manganese (Mn), 0.05 molybdenum (Mo), and 0.25 zinc (Zn).
Sole-source lighting treatments.
A multilayer (three layers) production system was used in the growth chamber for the establishment of SSL treatments. Commercially-available LED arrays providing radiation ratios of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8) (Philips GreenPower LED production modules; Koninklijke Philips Electronics, N.V., Netherlands) were mounted to one of nine stainless steel shelves (123 cm long and 61 cm wide). Nonreflective blackout cloth was used to prevent radiation pollution between treatments. Radiation intensity treatments were established by mounting 2, 4, or 6 modules, spaced 20.3, 12.2, or 8.6 cm apart, ≈38 cm above the crop canopy to achieve an average PPFD of 105, 210, or 315 µmol·m−2·s–1, respectively. A 16 h (0600 to 2200 hr) photoperiod provided plants with a DLI of 6.1, 12.1, or 18.1 mol·m−2·d−1, representing targets below, equal to, or above the recommended minimum target DLI of 10–12 mol·m−2·d−1, respectively (Pramuk and Runkle, 2005; Randall and Lopez, 2014). Radiation quality and PPFD were measured at the beginning and confirmed at the end of each experimental replication by taking nine individual spectral scans per treatment using a spectroradiometer (PS-100; StellarNet, Inc., Tampa, FL). Average PPFD and spectral qualities for each treatment are reported in Table 1 and Fig. 1, respectively. Trays were rotated within each treatment daily to reduce any positional effects on radiation distribution.
Average photosynthetic photon flux density (PPFD) from 400 to 700 nm ± sd delivered from sole-source light-emitting diodes (LEDs) with radiation ratios (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8) to achieve target radiation intensities of 105, 210, and 315 µmol·m−2·s–1. The average daily light integrals (DLIs), measured from 400 to 700 nm, under a 16 h photoperiod (0600 to 2200 hr) are also reported. Mean values reported are the average of nine spectral scans across the three experimental replications.
Spectral quality delivered from sole-source light-emitting diode (LED) arrays with radiation qualities (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8) at a photosynthetic photon flux density from 400 to 700 nm of 105, 210, or 315 µmol·m−2·s–1 at canopy level.
Citation: HortScience horts 53, 10; 10.21273/HORTSCI13228-18
Seedling data collection.
After 28 d under the SSL treatments, five experimental units (individual seedlings) from each treatment were randomly selected for measurements and analysis. Roots and shoots of the seedlings were washed, and nondestructive measurements were taken for stem length (cm; measured from the base of the hypocotyl to the shoot apical meristem) and stem caliper [mm; measured above the lowest leaf with a digital caliper (digiMax; Wiha, Schonach, Germany)]. Leaf area (cm2) was recorded using a leaf area meter (LI-3100; LI-COR Inc., Lincoln, NE) by removing the seedling leaves at the axil. Roots and shoots (leaves and stems) were then separated and placed in a drying oven at 70 °C for at least 4 d for the collection of root dry mass (RDM) and SDM. Additionally, stem length and caliper were used to calculate the sturdiness quotient (SQ; stem caliper/stem length) of each seedling. The quality index {QI; [total dry mass × (shoot:root ratio + sturdiness quotient)]} was then calculated according to Currey et al. (2013).
Nutrient analysis.
After 28 d, shoots of eight seedlings within each treatment were randomly collected, triple rinsed with deionized water, and placed in a drying oven at 70 °C for at least 4 d. Due to the limited dry mass obtained from a single seedling, eight seedlings provided a single sample for nutrient analysis, with five samples analyzed for each species within each treatment. Foliar N was determined using a CHN analyzer (PerkinElmer Series II CHNS/O Analyzer; PerkinElmer Instruments, Shelton, CT). For all other elements, plant tissue from each sample was digested in a microwave (MARS6; CEM Corp., Matthews, NC) and nutrient concentration was determined using inductively coupled plasma optical emission spectroscopy (ICP-OES; Thermo iCAP 6300; Thermo Electron Corp., Waltham, MA) as described by Frantz (2013).
Finishing environment.
After 28 d, five randomly selected seedlings from each treatment were transplanted into 11.4 cm (600 mL) containers (Dillen Products, Middlefield, OH) filled with a commercial soilless medium comprised of (by vol.) 75% peat, 20% perlite, and 5% vermiculite (Fafard 2; Sun Gro Horticulture) on 23 Dec. 2014 (Replication 1) and 11 Feb. 2015 (Replication 2). Plants were placed in a common finishing environment with an air temperature set point of 20 °C. An environmental control system (Maximizer Precision 10; Priva Computers Inc.) managed exhaust fan and evaporative-pad cooling, radiant hot water heating, and retractable shade curtains for the greenhouse. Solar PPFD was measured by quantum sensors (SQ-110; Apogee Instruments, Inc.) every 15 s and the average was logged every 15 min by a data logger (Model CR1000; Campbell Scientific, Inc.). Supplemental lighting was provided by 1000-W HPS lamps to assist in achieving a minimum DLI of 12 mol·m−2·d−1. Average daily temperature and DLI for the two experimental replications beginning on 23 Dec. 2014 and 11 Feb. 2015 were 20.2 ± 0.2 °C and 11.8 ± 2.8 mol·m−2·d−1 and 20.4 ± 0.7 °C and 14.5 ± 4.1 mol·m−2·d−1, respectively. When necessary, plants were irrigated with clear water alternating with fertigation using a combination of two water-soluble fertilizers (3:1 mixture of 15N–2.2P–12.5K and 21N–2.2P–16.6K; Everris, Marysville, OH) to provide the following (in mg·L−1): 200 N, 26 P, 163 K, 50 Ca, 20 Mg, 1.0 Fe, 0.5 Mn and Zn, 0.24 Cu and B, and 0.1 Mo.
Finishing environment data collection.
After transplant, plants were evaluated daily for first flower with all petals fully reflexed to calculate the TTF from the transplant date. Data were then collected on the number of nodes below the first open flower and SDM.
Statistical analysis.
The experiment was a completely randomized design with radiation quality (three levels) and radiation intensity (three levels) as factors and species evaluated separately. The experiment was repeated three times over time for the seedling data collection and twice over time for the finishing data collection. For each replication of the study, one 288-cell tray per species was subjected to each treatment, with individual seedlings within a tray serving as experimental units. The effects of radiation intensity and radiation quality were compared by ANOVA using SAS (SAS version 9.3; SAS Institute, Cary, NC) PROC MIXED and Tukey’s honest significant difference test at P ≤ 0.05. With the majority of variables displaying no significant interaction between radiation intensity and quality (Table 2), main effect means were reported (Tables 3 and 4). Additionally, the factors of radiation intensity and quality were evaluated separately. The effect of radiation intensity was compared within radiation qualities, while the effect of radiation quality was compared within radiation intensities for each species (data not shown).
Analysis of variance (ANOVA) for the effects of radiation quality (RQ), radiation intensity (RI), or RQ × RI from sole-source light-emitting diodes (LEDs) on propagation (28 d after germination) and finishing (transplanted 28 d after germination) for coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’).
Propagation (28 d after germination) and finishing (transplanted 28 d after germination) data for the main effect of radiation intensity including stem length, stem caliper, leaf area, root (RDM) and shoot dry mass (SDM), sturdiness quotient, quality index, time to flower, number of nodes below the first open flower, and SDM at flowering for coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’) seedlings grown under radiation intensities of 105, 210, or 315 µmol·m−2·s–1 delivered from sole-source light-emitting diodes (LEDs) during propagation.
Propagation (28 d after germination) and finishing (transplanted 28 d after germination) data for the main effect of radiation quality including stem length, stem caliper, leaf area, root (RDM) and shoot dry mass (SDM), sturdiness quotient, quality index, time to flower, number of nodes below the first open flower, and SDM at flowering for coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’) seedlings grown under radiation quality ratios (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8) delivered from sole-source light-emitting diodes (LEDs) during propagation.
Results
Stem length and caliper.
Stem length was 9%, 16%, and 21% shorter as radiation intensity increased from 105 to 315 µmol·m−2·s–1 for coreopsis, pansy, and petunia, respectively (Table 3). However, differences in stem length between the radiation intensities of 210 and 315 µmol·m−2·s–1 were only present for petunia. Specifically, stem length of petunia was 6% shorter at a radiation intensity of 315 compared with 210 µmol·m−2·s–1 (Table 3). Stem caliper increased 14%, 14%, and 10% for coreopsis, pansy, and petunia, respectively, at a radiation intensity of 315 compared with 105 µmol·m−2·s–1 (Table 3). Additionally, stem caliper of coreopsis increased 6% at a radiation intensity of 315 compared with 210 µmol·m−2·s–1 (Table 3). However, differences in stem caliper between the radiation intensities of 210 and 315 µmol·m−2·s–1 were not observed for pansy and petunia (Table 3).
Regarding radiation quality, stem length of pansy was 7% and 13% shorter under R87:B13 and R74:G18:B8, respectively, compared with R84:FR7:B9 (Table 4). Likewise, stem length of petunia was 15% shorter under R87:B13 compared with R84:FR7:B9. Stem caliper of coreopsis increased 12% and 9% under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively (Table 4). Additionally, stem caliper of petunia increased 13% and 11% under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively.
Leaf area.
As radiation intensity increased from 105 to 315 µmol·m−2·s–1, leaf area of petunia was 23% smaller (Table 3). Conversely, as radiation intensity increased from 105 to 315 µmol·m−2·s–1, leaf area of pansy was 16% larger. Regarding radiation quality, the largest leaf area was observed under R84:FR7:B9 for all three species (Table 4). Leaf area of pansy was 18% larger under R84:FR7:B9 compared with R87:B13, while leaf area of coreopsis and petunia was 29% and 15% larger and 27% and 14% larger under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively (Table 4).
RDM and SDM.
As radiation intensity increased, both RDM and SDM increased for all three species (Table 3). For example, as radiation intensity increased from 105 to 315 µmol·m−2·s–1, RDM of coreopsis, pansy, and petunia increased 269%, 245%, and 212%, respectively. Likewise, SDM of coreopsis, pansy, and petunia increased 90%, 131%, and 93%, respectively, as radiation intensity increased from 105 to 315 µmol·m−2·s–1. For coreopsis, RDM increased 26% and 19% under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively (Table 4). Additionally, SDM of coreopsis increased 33% and 22% under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively (Table 4). Likewise, SDM of petunia increased 23% under R84:FR7:B9 compared with R87:B13.
Quality parameters.
While radiation quality had little effect on quality parameters, seedlings grown under higher radiation intensities displayed higher SQ and QI values for all three species (Table 3). For example, SQ values for coreopsis, pansy, and petunia were 24%, 38%, and 41% higher, respectively, under the radiation intensity of 315 compared with 105 µmol·m−2·s–1. Similarly, QI values for all three species increased as radiation intensity increased (Table 3). Quality index values for coreopsis, pansy, and petunia were 255%, 231%, and 236% higher, respectively, under the radiation intensity of 315 compared with 105 µmol·m−2·s–1. In terms of radiation quality, QI values for coreopsis were 29% and 23% higher under R84:FR7:B9 compared with R87:B13 and R74:G18:B8, respectively (Table 4).
Nutrient concentration.
For all three species, both macro- and micronutrient concentrations were generally lower as radiation intensity increased (Tables 5 and 6). In terms of radiation quality, at a radiation intensity of 315 µmol·m−2·s–1, petunia accumulated 30%, 19%, 18%, 34%, and 25% more sulfur (S), Ca, Mg, Cu, and Zn, respectively, under R84:FR7:B9 compared with R74:G18:B8 (Tables 5 and 6). However, in pansy, the highest nutrient concentrations were often observed under R87:B13 (Tables 5 and 6). Specifically, at a radiation intensity of 105 µmol·m−2·s–1, pansy accumulated 12% more S and Mg under R87:B13 compared with R84:FR7:B9. Additionally, at a radiation intensity of 315 µmol·m−2·s–1, pansy accumulated 19% more S under R87:B13 compared with R74:G18:B8. Coreopsis displayed a similar trend to pansy at a radiation intensity of 105 µmol·m−2·s–1, with 9% more P and 20% more Mn for seedlings under R87:B13 compared with R84:FR7:B9 and R74:G18:B8, respectively (Tables 5 and 6).
Macronutrient concentration [percent dry mass (DM)] of coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’) seedlings 28 d after germination grown under radiation intensities (RIs) of 105, 210, or 315 µmol·m−2·s–1 delivered from sole-source light-emitting diodes (LEDs) with radiation quality (RQ) ratios (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8).
Micronutrient concentrations (mg·kg−1) of coreopsis (Coreopsis grandiflora ‘Sunfire’), pansy (Viola ×wittrockiana ‘Matrix Yellow’), and petunia (Petunia ×hybrida ‘Purple Wave’) seedlings 28 d after germination grown under radiation intensities (RIs) of 105, 210, or 315 µmol·m−2·s–1 delivered from sole-source light-emitting diodes (LEDs) with radiation quality (RQ) ratios (%) of red:blue 87:13 (R87:B13), red:far-red:blue 84:7:9 (R84:FR7:B9), or red:green:blue 74:18:8 (R74:G18:B8).
Finishing.
Pansy flowered an average of 5 and 4 d earlier when seedlings were grown at a radiation intensity of 210 or 315 µmol·m−2·s–1, respectively, compared with 105 µmol·m−2·s–1 (Table 3). Likewise, coreopsis flowered an average of 6 d earlier when seedlings were propagated at a radiation intensity of 315 compared with 105 µmol·m−2·s–1. Additionally, a decrease in TTF was observed in pansy and petunia seedlings grown under R84:FR7:B9 during propagation (Table 4). Pansy seedlings grown under R84:FR7:B9 flowered an average of 7 and 5 d earlier compared with R87:B13 and R74:G18:B8, respectively. Similarly, petunia seedlings grown under R84:FR7:B9 flowered an average of 2 d earlier compared with R87:B13.
For coreopsis and pansy, SDM at flower was 16% and 27% lower, respectively, when seedlings were propagated at a radiation intensity of 315 compared with 105 µmol·m−2·s–1 (Table 3). Regarding radiation quality, for pansy and petunia, the number of nodes at first flower was lower when seedlings were grown under R84:FR7:B9 (Table 4). For example, when pansy seedlings were grown under R84:FR7:B9, three fewer nodes were present at first flower compared with the other two radiation quality treatments. Similar results were observed for dry mass in pansy, with seedlings grown under R84:FR7:B9 possessing a 30% lower SDM at flower compared with R87:B13 (Table 4).
Discussion
A high-quality bedding plant seedling is one that has a compact habit, high RDM and SDM, and thick stem diameter (Oh et al., 2010; Pramuk and Runkle, 2005; Randall and Lopez, 2014). These qualitative parameters ultimately lead to seedlings that are more easily processed, shipped, and mechanically transplanted, which is desired by growers (Pramuk and Runkle, 2005). When produced in a growth chamber environment under SSL, we found that high radiation intensities and radiation qualities of R87:B13 and R74:G18:B8 generally led to compact seedlings with a shorter stem length and smaller leaf area compared with those grown under lower radiation intensities or with the inclusion of far-red wavelengths. High radiation intensities have been found to reduce the level of endogenous gibberellins (GAs) within higher plants, ultimately leading to reduced stem elongation and a more compact habit (Graebe, 1987; Potter et al., 1999). Thus, the compact seedling growth observed under higher radiation intensities was likely due to decreased GA levels. In the greenhouse, Lopez and Runkle (2008) reported comparable results as the shoot height of petunia ‘Tiny Tunia Violet Ice’, ‘Double Wave Spreading Rose’, and ‘Supertunia Mini Purple’ cuttings was 40%, 34%, and 55% taller, respectively, as the DLI decreased from 5.9 to 1.2 mol·m−2·d−1 with a 12 h photoperiod.
Far-red radiation is known to have a significant effect on promoting extension growth and leaf expansion (Downs and Thomas, 1982). Phytochromes are the photoreceptors responsible for detecting changes in the red:far-red (R:FR) ratio. In response to a lower R:FR ratio, many plants will display morphological changes such as increased stem elongation, larger leaf area, and thinner leaves, a response commonly referred to as shade avoidance (Franklin and Whitelam, 2005; Park and Runkle, 2017; Zhang and Folta, 2012). Park and Runkle (2017) found stem length of geranium ‘Pinto Premium Orange Bicolor’, petunia ‘Wave Blue’, snapdragon ‘Trailing Candy Showers Yellow’, and impatiens ‘Super Elfin XP Red’ seedlings displayed an inverse linear relationship with the estimated phytochrome photoequilibrium, which serves as an indicator of the relative amount of active phytochrome in plants, according to methods described by Sager et al. (1988). Specifically, as the estimated phytochrome photoequilibrium increased, stem length was shorter. Additionally, they found that leaf expansion was promoted for some species under a low R:FR ratio, as long as the radiation intensity was sufficient for growth. In the present study, the addition of FR radiation imbalanced the R:FR ratio under R84:FR7:B9 (R:FR = 9.3), and seedlings exhibited increased stem elongation and leaf area compared with R87:B13 and R74:G18:B8 as a result.
Blue radiation has been shown to inhibit growth for a variety of species (Cosgrove, 1981; Runkle and Heins, 2001). This is likely due to the blue radiation photoreceptor cryptochrome acting on one or more steps in the process of cell enlargement (Cosgrove, 1981; Kigel and Cosgrove, 1991; Runkle and Heins, 2001). Excessive hypocotyl elongation of seedlings has been reported under LED SSL containing high proportions of red radiation and little to no blue radiation (Hoenecke et al., 1992). Thus, blue radiation may be essential under SSL to minimize stem elongation and produce compact seedlings (Hoenecke et al., 1992; Wollaeger and Runkle, 2014).
Suppression of leaf area expansion under an increased percentage of blue radiation has previously been observed for petunia ‘Dreams Midnight’, impatiens ‘Super Elfin XP Blue Pearl’, and vinca ‘Titan Red Dark’ seedlings (Randall and Lopez, 2014). Wollaeger and Runkle (2015) found that ≈10 µmol·m−2·s–1 of blue radiation, in a spectrum of predominately red radiation, was sufficient to inhibit extension growth and leaf area expansion for impatiens ‘Super Elfin XP Red’, petunia ‘Wave Pink’, salvia ‘Vista Red’, and tomato (Solanum lycopersicum ‘Early Girl’) seedlings. This coincides with our findings in the present study, where petunia seedlings grown under lower radiation intensities displayed increased leaf area expansion and stem elongation under the radiation qualities of R84:FR7:B9 and R74:G18:B8 compared with R87:B13 (data not shown). Under the radiation qualities of R84:FR7:B9 and R74:G18:B8 at a radiation intensity of 105 µmol·m−2·s–1, the intensity of blue radiation was ≈9 and 8 µmol·m−2·s–1, respectively. However, the intensity of blue radiation under R87:B13, where differences in stem elongation and leaf area amongst radiation intensities were not observed, was ≈14 µmol·m−2·s–1 at a radiation intensity of 105 µmol·m−2·s–1. Franklin (2008) found that reductions in radiation intensity, specifically with regard to blue wavelengths, can elicit physiological responses characteristic of a low R:FR ratio. Therefore, it is likely that with lower radiation intensities, seedlings grown under reduced percentages of blue radiation were not exposed to a sufficient quantity to inhibit responses connected to shade avoidance.
For many commercial LED arrays, a small percentage of green wavelengths is commonly included in the spectrum to facilitate crop assessment and provide a more comfortable environment for workers in controlled environments. While green radiation has traditionally been deemed as less efficient than blue or red radiation for the promotion of plant growth, recent studies have found that green wavelengths may penetrate deeper into leaves and canopies to improve productivity and manipulate stomatal aperture (Smith et al., 2017). Additionally, green radiation absorbed by cryptochrome has been found to stimulate a response similar to shade avoidance, as these wavelengths can reverse the effects of blue radiation-inhibited hypocotyl elongation (Smith et al., 2017; Zhang and Folta, 2012). While this mechanism is not fully understood, the addition of green radiation may have also resulted in the increased leaf area and stem elongation observed with petunia under R74:G18:B8 compared with R87:B13 at low radiation intensities (data not shown). Additionally, the larger leaf area observed with coreopsis under R74:G18:B8 compared with R87:B13 was likely a similar response.
For all three species in the present study, both RDM and SDM increased under higher radiation intensities. This observation is well documented, with many greenhouse studies reporting an increased DLI leading to increased biomass accumulation and growth rate (Graper and Healy, 1991, 1992; Lopez and Runkle, 2008; Pramuk and Runkle, 2005). For example, Oh et al. (2010) found that pansy ‘Delta Premium Yellow’ and petunia ‘Madness Red’ seedlings displayed a linear increase in SDM under increasing DLIs. In the present study, both RDM and SDM for all three species continued to significantly increase up to the highest radiation intensity of 315 µmol·m−2·s–1. Thus, while it is generally recommended that seedlings be grown at a DLI of 10 to 12 mol·m−2·d−1 (175 to 210 µmol·m−2·s–1 with a 16 h photoperiod), potential increases in seedling quality and a decrease in production time may be possible under higher radiation intensities. However, whether increased radiation intensity provides an economic benefit for the production of bedding plant seedlings remains uncertain.
Root dry mass and SDM of seedlings grown under R84:FR7:B9 were often higher than seedlings grown under R87:B13 or R74:G18:B8. Wollaeger and Runkle (2014) suggest the primary role of radiation quality on biomass accumulation in tomato ‘Early Girl’, salvia ‘Vista Red’, impatiens ‘Super Elfin XP Red’, and petunia ‘Wave Pink’ seedlings can be attributed to an increase in leaf area. As leaf area increases, the potential for biomass accumulation also increases due to a greater potential for radiation interception. Leaf area was largest under R84:FR7:B9 for all three species in the present study. Therefore, it is likely that the addition of far-red wavelengths allowed for an increase in leaf area by lowering the R:FR ratio, ultimately leading to increased radiation interception and SDM accumulation. In addition to increasing leaf area, the inclusion of far-red radiation may have enhanced the total photosynthetically active radiation (PAR) available to the seedlings. Li and Kubota (2009) found that fluorescent white radiation supplemented with far-red LEDs led to increased fresh and dry weight of lettuce (Lactuca sativa ‘Red Cross’) compared with fluorescent radiation alone at the same PPFD. Increasing the quantum yield with far-red radiation has also been shown to increase whole-plant net assimilation for multiple bedding plant species (Park and Runkle, 2016, 2017). Recent studies have also shown that photosynthetic activity in photosystem II (PSII) can be stimulated by far-red radiation (Pettai et al., 2005; Thapper et al., 2009; Zhen and van Iersel, 2017). In the present study, target radiation intensities were achieved by accounting for PAR rather than total photon flux (TPF; 400–800 nm). Thus, the radiation intensities established using the R84:FR7:B9 LEDs did not account for the additional 7% far-red radiation (≈7–22 µmol·m−2·s–1). As the impacts of far-red radiation continue to be researched, future studies may need to use TPF rather than PPFD to measure the amount of radiation available for photosynthetic activity.
The QI provides an objective, integrated, and quantitative measurement for further evaluation of seedling quality, with higher values indicating higher quality (Currey et al., 2013; Randall and Lopez, 2014). The highest quality seedlings were consistently produced under higher radiation intensities, with little to no effect from radiation quality. This increased quality was primarily due to seedlings grown under higher radiation intensities exhibiting shorter stems, larger stem calipers, and higher RDM and SDM.
Both macro- and micronutrient concentrations were generally lowest in seedlings grown under high radiation intensities. Similar to observations made by Gerovac et al. (2016), this trend may be the result of a dilution of nutrients due to the higher SDM consistently found at higher radiation intensities (Table 3). Kuehny et al. (1991) previously investigated this effect of nutrient dilution in chrysanthemum (Chrysanthemum ×morifolium ‘Fiesta’) and found that foliar concentrations of nutrients were lower under increased irradiance and an elevated CO2 concentration. However, when data were expressed on a starch-free dry weight basis, the authors found that most of the differences observed between treatments were no longer apparent (Kuehny et al., 1991). Therefore, it is plausible that seedlings grown under the lower radiation intensities in the present study were more nutrient dense simply due to reduced biomass accumulation.
Radiation quality also influenced nutrient concentration. Specifically, for both coreopsis and pansy, select macro- and micronutrients were significantly higher under R87:B13 compared with R84:FR7:B9 and R74:G18:B8. An increased percentage of blue radiation has been found to result in higher concentrations of essential elements in microgreens (Kopsell and Sams, 2013; Kopsell et al., 2014). Kopsell et al. (2014) proposed that blue radiation plays a dominant role in regulating processes linked to nutrient content, including membrane permeability, proton pumping, and ion channel activities. Additionally, blue radiation has been found to play a primary role in the regulation of stomatal opening (Kinoshita et al., 2001; Van Ieperen et al., 2012), which may directly affect nutrient uptake via transpirationally-induced mass flow. Therefore, the increase in select macro- and micronutrients for coreopsis and pansy under R87:B13 LEDs may have resulted from the 4% to 5% increase in blue radiation compared with the other two treatments.
The effects of DLI on flowering in greenhouse-grown bedding plant species is well documented (Faust et al., 2005; Oh et al., 2010; Pramuk and Runkle, 2005). Pramuk and Runkle (2005) found that TTF for celosia ‘Gloria Mix’, impatiens ‘Accent Red’, salvia ‘Vista Red’, marigold ‘Bonanza Yellow’, and pansy ‘Crystal Bowl Yellow’ decreased as the greenhouse DLI increased during propagation. Additionally, these authors reported that the percentage of impatiens ‘Accent Red’ and marigold ‘Bonanza Yellow’ seedlings with visible bud at transplant also increased as the DLI increased (Pramuk and Runkle, 2005). Lopez and Runkle (2008) found a similar decrease in TTF for petunia ‘Tiny Tunia Violet’ and ‘Supertunia Mini Purple’ as the greenhouse DLI increased from 1.4 to 10.7 mol·m−2·d−1 during cutting propagation. Plants exhibiting a facultative irradiance response tend to flower earlier and develop fewer nodes before flower initiation when exposed to higher radiation environments (Erwin et al., 2017). In the present study, both coreopsis and pansy possessed a facultative irradiance response as exhibited by their earlier flowering and lower number of nodes at flower. One limitation to this conclusion may have been increased leaf temperatures under higher radiation intensities. However, while leaf temperature was not measured in the present study, similar research (data not shown) has found that leaf temperature of petunia ‘Dreams Midnight’ differed less than 0.5 °C between sole-source LED radiation intensities of 150 and 300 µmol·m−2·s−1 and varying red:blue radiation ratios. Thus, the earlier flowering response observed for coreopsis and pansy was likely due to differences in radiation intensity rather than leaf temperature.
With coreopsis and pansy, lower SDM at first flower was observed as the radiation intensity increased. Hutchinson et al. (2012) found similar results: TTF for Angelonia angustifolia ‘AngelMist White Cloud’ and Osteospermum ecklonis ‘Voltage Yellow’ decreased linearly as the DLI during propagation increased, with lower SDM values observed alongside this decrease in days to flower. Earlier flowering may be beneficial when seedlings are produced with the intent for finishing in small containers, while a delay in flowering would likely be preferred for seedlings intended for large containers, as this would encourage increased vegetative development (Hutchinson et al., 2012; Mattson and Erwin, 2005).
For pansy, TTF significantly decreased when seedlings were grown under R84:FR7:B9 compared with the other radiation quality treatments. Far-red radiation has been shown to have a significant effect on the promotion of flowering for plants with a long-day photoperiodic response (Downs and Thomas, 1982). However, species with a long-day photoperiodic response may respond differently to the inclusion or exclusion of far-red radiation. For some species, the response to far-red radiation is specific to flower development, while in others the effect is specific to flower induction (Runkle and Heins, 2001; Thomas and Vince-Prue, 1997). For coreopsis and petunia, it is likely that far-red radiation was unnecessary for flower induction, leading to only minor differences observed in TTF with the inclusion of these wavelengths. However, the inclusion of far-red radiation led to a significant decrease in TTF for pansy, leading to the assumption that flower induction was accelerated during propagation under R84:FR7:B9. Park and Runkle (2017) found similar results in that only one of two species evaluated with a long-day photoperiodic response was responsive to the inclusion of far-red radiation during seedling production for earlier flowering. However, both species displayed increased growth and characteristic photomorphogenic responses to the inclusion of far-red radiation. Thus, these authors concluded that the regulation of flowering and photomorphogenic responses from far-red radiation are independent within the plant (Park and Runkle, 2017). While all three species displayed photomorphogenic responses to far-red radiation in the present study, pansy was the only species that possessed a flowering response. Thus, the characterization and selection of species responses to the inclusion or exclusion of various wavelengths of radiation is critical when designing SSL applications.
Based on our results, radiation intensity appears to be the dominant factor influencing seedling quality under SSL. While radiation quality can induce a variety of photomorphogenic responses, the highest quality seedlings for all three species were consistently produced under the radiation intensity of 315 µmol·m−2·s−1. Thus, for most production applications, priority should be placed on PPFD rather than spectral composition. However, it is important to note that the LED arrays used for this study were commercially available fixtures with spectral ratios predetermined by the manufacturer. While the prospect of reducing the radiation intensity under optimized spectra does exist, further research is required to elucidate these spectral responses for seedling production. Nevertheless, far-red wavelengths included in the spectrum may be beneficial if accelerated flowering upon transplant is desired for long-day plants, but this response is highly dependent on species. Therefore, these results provide further information regarding the specific radiation parameters from commercially available LEDs necessary to produce high-quality bedding plant seedlings under SSL.
Literature Cited
Barnes, C., Tibbitts, T., Sager, J., Deitzer, G., Bubenheim, D., Koerner, G. & Bugbee, B. 1993 Accuracy of quantum sensors measuring yield photon flux and photosynthetic photon flux HortScience 28 1197 1200
Cope, K.R., Snowden, M.C. & Bugbee, B. 2014 Photobiological interactions of blue light and photosynthetic photon flux: Effects of monochromatic and broad-spectrum light sources Photochem. Photobiol. 90 574 584
Cosgrove, D.J. 1981 Rapid suppression of growth by blue light Plant Physiol. 67 584 590
Currey, C.J., Torres, A.P., Lopez, R.G. & Jacobs, D.F. 2013 The quality index – a new tool for integrating quantitative measurements to assess quality of young floriculture plants Acta Hort. 1000 385 391
Currey, C.J., Lopez, R.G. & Mattson, N.S. 2011 Flower induction of annuals. Purdue Ext. Bul. H0-249-W
Downs, R.J. & Thomas, J.F. 1982 Phytochrome regulation of flowering in the long-day plant, Hyoscyamus niger Plant Physiol. 70 898 900
Erwin, J., Mattson, N. & Warner, R. 2017 Light effects on bedding plants, p. 119−134. In: R. Lopez and E. Runkle (eds.). Light management in controlled environments. Meister Media Worldwide, Willoughby, OH
Faust, J.E., Holcombe, V., Rajapakse, N.C. & Layne, D.R. 2005 The effect of daily light integral on bedding plant growth and flowering HortScience 40 645 649
Franklin, K.A. 2008 Shade avoidance New Phytol. 179 930 944
Franklin, K.A. & Whitelam, G.C. 2005 Phytochromes and shade-avoidance responses in plants Ann. Bot. 96 169 175
Frantz, J.M. 2013 Uptake efficiency of phosphorus in different light environments by zinnia (Zinnia elegans) and vinca (Catharanthus roseus) HortScience 48 594 600
Gerovac, J.R., Craver, J.K., Boldt, J.K. & Lopez, R.G. 2016 Radiation intensity and quality from sole-source light-emitting diodes impact growth, morphology, and nutrient content of Brassica microgreens HortScience 5 497 503
Graebe, J.E. 1987 Gibberellin biosynthesis and control Annu. Rev. Plant Physiol. 38 419 465
Graper, D.F. & Healy, W. 1991 High pressure sodium irradiation and infrared radiation accelerate petunia seedling growth J. Amer. Soc. Hort. Sci. 116 435 438
Graper, D.F. & Healy, W. 1992 Modification of petunia seedling carbohydrate partitioning by irradiance J. Amer. Soc. Hort. Sci. 117 477 480
Hoenecke, M.E., Bula, R.J. & Tibbits, T.W. 1992 Importance of ‘blue’ photon levels for lettuce seedlings grown under red-light-emitting diodes HortScience 27 427 430
Hutchinson, V.A., Currey, C.J. & Lopez, R.G. 2012 Photosynthetic daily light integral during root development influences subsequent growth and development of several herbaceous annual bedding plants HortScience 47 856 860
Kigel, J. & Cosgrove, D.J. 1991 Photoinhibition of stem elongation by blue and red light Plant Physiol. 95 1049 1056
Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M. & Shimazaki, K. 2001 Phot1 and phot2 mediate blue light regulation of stomatal opening Nature 414 656 660
Kopsell, D.A. & Sams, C.E. 2013 Increase in shoot tissue pigments, glucosinolates, and mineral elements in sprouting broccoli after exposure to short-duration blue light from light-emitting diodes J. Amer. Soc. Hort. Sci. 138 31 37
Kopsell, D.A., Sams, C.E., Barickman, T.C. & Morrow, R.C. 2014 Sprouting broccoli accumulate higher concentrations of nutritionally important metabolites under narrow-band light-emitting diode lighting J. Amer. Soc. Hort. Sci. 139 469 477
Kuehny, J.S., Peet, M.M., Nelson, P.V. & Willits, D.H. 1991 Nutrient dilution by starch in CO2-enriched chrysanthemum J. Expt. Bot. 42 711 716
Li, Q. & Kubota, C. 2009 Effects of supplemental radiation quality on growth and phytochemicals of baby leaf lettuce Environ. Exp. Bot. 67 59 64
Lopez, R., Currey, C. & Runkle, E. 2017 Light and young plants, p. 109−118. In: R. Lopez and E. Runkle (ed.). Light management in controlled environments. Meister Media Worldwide, Willoughby, OH
Lopez, R.G. & Runkle, E.S. 2008 Photosynthetic daily light integral during propagation influences rooting and growth of cuttings and subsequent development of New Guinea impatiens and petunia HortScience 43 2052 2059
Massa, G.D., Kim, H., Wheeler, R.M. & Mitchell, C.A. 2008 Plant productivity in response to LED lighting HortScience 43 1951 1956
Mattson, N.S. & Erwin, J.E. 2005 The impact of photoperiod and irradiance on flowering of several herbaceous ornamentals Scientia Hort. 104 275 292
Mitchell, C.A., Both, A., Bourget, C.M., Burr, J.F., Kubota, C., Lopez, R.G., Morrow, R.C. & Runkle, E.S. 2012 LEDs: The future of greenhouse lighting! Chronica Hort. 52 6 12
Oh, W., Runkle, E.S. & Warner, R.M. 2010 Timing and duration of supplemental lighting during the seedling stage influence quality and flowering in petunia and pansy HortScience 45 1332 1337
Park, Y. & Runkle, E.S. 2016 Investigating the merit of including far-red radiation in the production of ornamental seedlings grown under sole-source lighting Acta Hort. 1134 259 266
Park, Y. & Runkle, E.S. 2017 Far-red radiation promotes growth of seedlings by increasing leaf expansion and whole-plant net assimilation Environ. Expt. Bot. 136 41 49
Pettai, H., Oja, V., Freiberg, A. & Lasik, A. 2005 Photosynthetic activity of far-red light in green plants Biochim. Biophys. Acta 1708 311 321
Potter, T.I., Rood, S.B. & Zanewich, K.P. 1999 Radiation intensity, gibberellin content and the resolution of shoot growth in Brassica Planta 207 505 511
Pramuk, L.A. & Runkle, E.S. 2005 Photosynthetic daily light integral during the seedling stage influences subsequent growth and flowering of Celosia, Impatiens, Salvia, Tagetes, and Viola HortScience 40 1336 1339
Randall, W.C. & Lopez, R.G. 2014 Comparison of supplemental lighting from high-pressure sodium lamps and light-emitting diodes during bedding plant seedling production HortScience 49 589 595
Randall, W.C. & Lopez, R.G. 2015 Comparison of bedding plant seedlings grown under sole-source light-emitting diodes (LEDs) and greenhouse supplemental lighting from LEDs and high-pressure sodium lamps HortScience 50 705 713
Runkle, E.S. & Heins, R.D. 2001 Specific functions of red, far red, and blue light in flowering and stem extension of long-day plants J. Amer. Soc. Hort. Sci. 126 275 282
Sager, J.C., Smith, W.O., Edwards, J.L. & Cyr, K.L. 1988 Photosynthetic efficiency and phytochrome photoequilibria determination using spectral data. Trans. Amer. Soc. Agr. Eng. 31:1882–1889
Smith, H.L., McAusland, L. & Murchie, E.H. 2017 Don’t ignore the green light: Exploring diverse roles in plant processes J. Expt. Bot. 68 2099 2110
Stutte, G.W. 2009 Light-emitting diodes for manipulating the phytochrome apparatus HortScience 44 231 234
Styer, R.C. 2003 Propagating seed crops, p. 151–163. In: D. Hamrick (ed.). Ball redbook crop production: Vol. 2. 17th ed. Ball Publishing, Batavia, IL
Thapper, A., Mamedov, F., Mokvist, F., Hammarstrom, L. & Styring, S. 2009 Defining the far-red limit of photosystem II in spinach Plant Cell 21 2391 2401
Thomas, B. & Vince-Prue, D. 1997 Photoperiodism in plants. 2nd ed. Academic Press, London
Van Ieperen, W., Savvides, A. & Fanourakis, D. 2012 Red and blue light effects during growth on hydraulic and stomatal conductance in leaves of young cucumber plants Acta Hort. 956 223 230
Wollaeger, H.M. & Runkle, E.S. 2014 Producing commercial-quality ornamental seedlings under sole-source LED lighting Acta Hort. 1037 269 276
Wollaeger, H.M. & Runkle, E.S. 2015 Growth and acclimation of impatiens, salvia, petunia, and tomato seedlings to blue and red light HortScience 50 522 529
Zhang, T. & Folta, K. 2012 Green light signaling and adaptive response Plant Signal. Behav. 7 1 4
Zhen, S. & van Iersel, M.W. 2017 Far-red light is needed for efficient photochemistry and photosynthesis J. Plant Physiol. 209 115 122